A protective role of ciglitazone in ox-LDL-induced rat microvascular endothelial cells via modulating PPARγ-dependent AMPK/eNOS pathway

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 1, 2015, Pages 92-102

  Xu, Lei ^a   Wang, Shijun ^a   Li, Bingyu ^a   Sun, Aijun ^a   Zou, Yunzeng ^a   Ge, Junbo ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

eNOS; AMPK; Angiogenesis; Endothelial cells; LOX 1; PPAR

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; CIGLITAZONE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LOW DENSITY LIPOPROTEIN; OLR1 PROTEIN, MOUSE; OXIDIZED LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTECTIVE AGENT;

ANIMAL; BIOLOGICAL MODEL; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYMOLOGY; IN VITRO STUDY; MALE; METABOLISM; MICROVASCULATURE; MOLECULAR GENETICS; PATHOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; IN VITRO TECHNIQUES; LIPOPROTEINS, LDL; MALE; MICROVESSELS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NITRIC OXIDE SYNTHASE TYPE III; PPAR GAMMA; PROTECTIVE AGENTS; RATS, WISTAR; SCAVENGER RECEPTORS, CLASS E; SIGNAL TRANSDUCTION; THIAZOLIDINEDIONES;

EID: 84921458646     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12463     Document Type: Article

References (58)

1. Zeiher AM, Drexler H, Wollschlager H, et al. Modulation of coronary vasomotor tone in humans. Progressive endothelial dysfunction with different early stages of coronary atherosclerosis. Circulation. 1991; 83: 391-401.
2. Reddy KG, Nair RN, Sheehan HM, et al. Evidence that selective endothelial dysfunction may occur in the absence of angiographic or ultrasound atherosclerosis in patients with risk factors for atherosclerosis. J Am Coll Cardiol. 1994; 23: 833-43.
3. Anderson TJ, Gerhard MD, Meredith IT, et al. Systemic nature of endothelial dysfunction in atherosclerosis. The American journal of cardiology. 1995; 75: 71B-4B.
4. Forstermann U, Pollock JS, Nakane M. Nitric oxide synthases in the cardiovascular system. Trends Cardiovasc Med. 1993; 3: 104-10.
5. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA. 1991; 88: 4651-5.
6. Provost P, Lam JY, Lacoste L, et al. Endothelium-derived nitric oxide attenuates neutrophil adhesion to endothelium under arterial flow conditions. Arterioscler Thromb. 1994; 14: 331-5.
7. Gauthier TW, Scalia R, Murohara T, et al. Nitric oxide protects against leukocyte-endothelium interactions in the early stages of hypercholesterolemia. Arterioscler Thromb Vasc Biol. 1995; 15: 1652-9.
8. Park CW, Kim HW, Lim JH, et al. Vascular endothelial growth factor inhibition by dRK6 causes endothelial apoptosis, fibrosis, and inflammation in the heart via the Akt/eNOS axis in db/db mice. Diabetes. 2009; 58: 2666-76.
9. Edirisinghe I, Yang SR, Yao H, et al. VEGFR-2 inhibition augments cigarette smoke-induced oxidative stress and inflammatory responses leading to endothelial dysfunction. FASEB J. 2008; 22: 2297-310.
10. Huang PL, Huang Z, Mashimo H, et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature. 1995; 377: 239-42.
11. d'Uscio LV, Smith LA, Santhanam AV, et al. Essential role of endothelial nitric oxide synthase in vascular effects of erythropoietin. Hypertension. 2007; 49: 1142-8.
12. Ge J, Huang D, Liang C, et al. Upregulation of lectinlike oxidized low-density lipoprotein receptor-1 expression contributes to the vein graft atherosclerosis: modulation by losartan. Atherosclerosis. 2004; 177: 263-8.
13. Luo Y, Liang C, Xu C, et al. Ciglitazone inhibits oxidized-low density lipoprotein induced immune maturation of dendritic cells. J Cardiovasc Pharmacol. 2004; 44: 381-5.
14. Ge J, Jia Q, Liang C, et al. Advanced glycosylation end products might promote atherosclerosis through inducing the immune maturation of dendritic cells. Arterioscler Thromb Vasc Biol. 2005; 25: 2157-63.
15. Sun A, Liu H, Wang S, et al. Salvianolic acid B suppresses maturation of human monocyte-derived dendritic cells by activating PPARgamma. Br J Pharmacol. 2011; 164: 2042-53.
16. Liu H, Wang S, Sun A, et al. Danhong inhibits oxidized low-density lipoprotein-induced immune maturation of dentritic cells via a peroxisome proliferator activated receptor gamma-mediated pathway. J Pharm Sci. 2012; 119: 1-9.
17. Shiu SW, Wong Y, Tan KC. Effect of advanced glycation end products on lectin-like oxidized low density lipoprotein receptor-1 expression in endothelial cells. J Atheroscler Thromb. 2012; 19: 1083-92.
18. Liang C, Ren Y, Tan H, et al. Rosiglitazone via upregulation of Akt/eNOS pathways attenuates dysfunction of endothelial progenitor cells, induced by advanced glycation end products. Br J Pharmacol. 2009; 158: 1865-73.
19. Ryan MJ, Didion SP, Mathur S, et al. PPAR(gamma) agonist rosiglitazone improves vascular function and lowers blood pressure in hypertensive transgenic mice. Hypertension. 2004; 43: 661-6.
20. Howarth AG, Wiehler WB, Pannirselvam M, et al. A nonthiazolidinedione peroxisome proliferator-activated receptor gamma agonist reverses endothelial dysfunction in diabetic (db/db-/-) mice. J Pharmacol Exp Ther. 2006; 316: 364-70.
21. Gonon AT, Bulhak A, Labruto F, et al. Cardioprotection mediated by rosiglitazone, a peroxisome proliferator-activated receptor gamma ligand, in relation to nitric oxide. Basic Res Cardiol. 2007; 102: 80-9.
22. Kobayashi N, Ohno T, Yoshida K, et al. Cardioprotective mechanism of telmisartan via PPAR-gamma-eNOS pathway in dahl salt-sensitive hypertensive rats. Am J Hypertens. 2008; 21: 576-81.
23. Fleming I, Mohamed A, Galle J, et al. Oxidized low-density lipoprotein increases superoxide production by endothelial nitric oxide synthase by inhibiting PKCalpha. Cardiovasc Res. 2005; 65: 897-906.
24. Xie L, Liu Z, Lu H, et al. Pyridoxine inhibits endothelial NOS uncoupling induced by oxidized low-density lipoprotein via the PKCalpha signalling pathway in human umbilical vein endothelial cells. Br J Pharmacol. 2012; 165: 754-64.
25. Huang D, Lu H, Liu H, et al. Losartan attenuates human monocyte-derived dendritic cell immune maturation via downregulation of lectin-like oxidized low-density lipoprotein receptor-1. J Cardiovasc Pharmacol. 2012; 60: 133-9.
26. Zou MH, Kirkpatrick SS, Davis BJ, et al. Activation of the AMP-activated protein kinase by the anti-diabetic drug metformin in vivo. Role of mitochondrial reactive nitrogen species. J Biol Chem. 2004; 279: 43940-51.
27. Ishii N, Matsumura T, Kinoshita H, et al. Activation of AMP-activated protein kinase suppresses oxidized low-density lipoprotein-induced macrophage proliferation. J Biol Chem. 2009; 284: 34561-9.
28. Chen ZP, Mitchelhill KI, Michell BJ, et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999; 443: 285-9.
29. Zhang Y, Lee TS, Kolb EM, et al. AMP-activated protein kinase is involved in endothelial NO synthase activation in response to shear stress. Arterioscler Thromb Vasc Biol. 2006; 26: 1281-7.
30. Brandes RP, Koddenberg G, Gwinner W, et al. Role of increased production of superoxide anions by NAD(P)H oxidase and xanthine oxidase in prolonged endotoxemia. Hypertension. 1999; 33: 1243-9.
31. Wang K, Brems JJ, Gamelli RL, et al. iNOS/NO signaling regulates apoptosis induced by glycochenodeoxycholate in hepatocytes. Cell Signal. 2011; 23: 1677-85.
32. Reihill JA, Ewart MA, Hardie DG, et al. AMP-activated protein kinase mediates VEGF-stimulated endothelial NO production. Biochem Biophys Res Commun. 2007; 354: 1084-8.
33. Levine YC, Li GK, Michel T. Agonist-modulated regulation of AMP-activated protein kinase (AMPK) in endothelial cells. Evidence for an AMPK -> Rac1 -> Akt -> endothelial nitric-oxide synthase pathway. J Biol Chem. 2007; 282: 20351-64.
34. Nizamutdinova IT, Kim YM, Kim HJ, et al. Carbon monoxide (from CORM-2) inhibits high glucose-induced ICAM-1 expression via AMP-activated protein kinase and PPAR-gamma activations in endothelial cells. Atherosclerosis. 2009; 207: 405-11.
35. Tsai KL, Chen LH, Chiou SH, et al. Coenzyme Q10 suppresses oxLDL-induced endothelial oxidative injuries by the modulation of LOX-1-mediated ROS generation via the AMPK/PKC/NADPH oxidase signaling pathway. Mol Nutr Food Res. 2011; 55: S227-40.
36. Zhou J, Abid MD, Xiong Y, et al. ox-LDL downregulates eNOS activity via LOX-1-mediated endoplasmic reticulum stress. Int J Mol Med. 2013; 32: 1442-50.
37. Smirnova IV, Sawamura T, Goligorsky MS. Upregulation of lectin-like oxidized low-density lipoprotein receptor-1 (LOX-1) in endothelial cells by nitric oxide deficiency. Am J Physiol Renal Physiol. 2004; 287: F25-32.
38. Mehta JL, Li DY, Chen HJ, et al. Inhibition of LOX-1 by statins may relate to upregulation of eNOS. Biochem Biophys Res Commun. 2001; 289: 857-61.
39. Calnek DS, Mazzella L, Roser S, et al. Peroxisome proliferator-activated receptor gamma ligands increase release of nitric oxide from endothelial cells. Arterioscler Thromb Vasc Biol. 2003; 23: 52-7.
40. Polikandriotis JA, Mazzella LJ, Rupnow HL, et al. Peroxisome proliferator-activated receptor gamma ligands stimulate endothelial nitric oxide production through distinct peroxisome proliferator-activated receptor gamma-dependent mechanisms. Arterioscler Thromb Vasc Biol. 2005; 25: 1810-6.
41. Aoki C, Suzuki K, Yanagi K, et al. Miglitol, an anti-diabetic drug, inhibits oxidative stress-induced apoptosis and mitochondrial ROS over-production in endothelial cells by enhancement of AMP-activated protein kinase. J Pharm Sci. 2012; 120: 121-8.
42. Wang XF, Zhang JY, Li L, et al. Metformin improves cardiac function in rats via activation of AMP-activated protein kinase. Clin Exp Pharmacol Physiol. 2011; 38: 94-101.
43. Zhang CX, Pan SN, Meng RS, et al. Metformin attenuates ventricular hypertrophy by activating the AMP-activated protein kinase-endothelial nitric oxide synthase pathway in rats. Clin Exp Pharmacol Physiol. 2011; 38: 55-62.
44. Cao X, Li H, Tao H, et al. Metformin inhibits vascular calcification in female rat aortic smooth muscle cells via the AMPK-eNOS-NO pathway. Endocrinology. 2013; 154: 3680-9.
45. Teng RJ, Du J, Afolayan AJ, et al. AMP kinase activation improves angiogenesis in pulmonary artery endothelial cells with in utero pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2013; 304: L29-42.
46. Aschner JL, Foster SL, Kaplowitz M, et al. Heat shock protein 90 modulates endothelial nitric oxide synthase activity and vascular reactivity in the newborn piglet pulmonary circulation. Am J Physiol Lung Cell Mol Physiol. 2007; 292: L1515-25.
47. Sud N, Sharma S, Wiseman DA, et al. Nitric oxide and superoxide generation from endothelial NOS: modulation by HSP90. Am J Physiol Lung Cell Mol Physiol. 2007; 293: L1444-53.
48. Cheng J, Ou JS, Singh H, et al. 20-hydroxyeicosatetraenoic acid causes endothelial dysfunction via eNOS uncoupling. Am J Physiol Heart Circ Physiol. 2008; 294: H1018-26.
49. Hu Z, Chen J, Wei Q, et al. Bidirectional actions of hydrogen peroxide on endothelial nitric-oxide synthase phosphorylation and function: co-commitment and interplay of Akt and AMPK. J Biol Chem. 2008; 283: 25256-63.
50. Stahmann N, Woods A, Spengler K, et al. Activation of AMP-activated protein kinase by vascular endothelial growth factor mediates endothelial angiogenesis independently of nitric-oxide synthase. J Biol Chem. 2010; 285: 10638-52.
51. Argmann CA, Sawyez CG, McNeil CJ, et al. Activation of peroxisome proliferator-activated receptor gamma and retinoid X receptor results in net depletion of cellular cholesteryl esters in macrophages exposed to oxidized lipoproteins. Arterioscler Thromb Vasc Biol. 2003; 23: 475-82.
52. Martinelli R, Gegg M, Longbottom R, et al. ICAM-1-mediated endothelial nitric oxide synthase activation via calcium and AMP-activated protein kinase is required for transendothelial lymphocyte migration. Mol Biol Cell. 2009; 20: 995-1005.
53. Mita S, Kobayashi N, Yoshida K, et al. Cardioprotective mechanisms of Rho-kinase inhibition associated with eNOS and oxidative stress-LOX-1 pathway in Dahl salt-sensitive hypertensive rats. J Hypertens. 2005; 23: 87-96.
54. Kobayashi N, Honda T, Yoshida K, et al. Critical role of bradykinin-eNOS and oxidative stress-LOX-1 pathway in cardiovascular remodeling under chronic angiotensin-converting enzyme inhibition. Atherosclerosis. 2006; 187: 92-100.
55. Taye A, Saad AH, Kumar AH, et al. Effect of apocynin on NADPH oxidase-mediated oxidative stress-LOX-1-eNOS pathway in human endothelial cells exposed to high glucose. Eur J Pharmacol. 2010; 627: 42-8.
56. Gonon AT, Widegren U, Bulhak A, et al. Adiponectin protects against myocardial ischaemia-reperfusion injury via AMP-activated protein kinase, Akt, and nitric oxide. Cardiovasc Res. 2008; 78: 116-22.
57. Wong WT, Tian XY, Xu A, et al. Adiponectin is required for PPARgamma-mediated improvement of endothelial function in diabetic mice. Cell Metab. 2011; 14: 104-15.
58. Chen X, Zhang H, McAfee S, et al. The reciprocal relationship between adiponectin and LOX-1 in the regulation of endothelial dysfunction in ApoE knockout mice. Am J Physiol Heart Circ Physiol. 2010; 299: H605-12.